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Pulse Register Phonation in Diana Monkey Alarm Calls

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Pulse Register Phonation in Diana Monkey Alarm Calls View metadata, citation and similarPublished papers inat core.ac.ukThe Journal of the Acoustical Society of America, Vol. 113, Issue 5, 2003, p. 2919-2926 brought to you by CORE which should be used for any reference to this work provided by RERO DOC1 Digital Library Pulse register phonation in Diana monkey alarm calls Tobias Riedea) Department of Psychology, 245 Uris Hall, Cornell University, Ithaca, New York 14853 Klaus Zuberbu¨hlerb) School of Psychology, University of St. Andrews, St. Andrews, Fife KY 16 9JU, Scotland, United Kingdom The adult male Diana monkeys ͑Cercopithecus diana͒ produce predator-specific alarm calls in response to two of their predators, the crowned eagles and the leopards. The acoustic structure of these alarm calls is remarkable for a number of theoretical and empirical reasons. First, although pulsed phonation has been described in a variety of mammalian vocalizations, very little is known about the underlying production mechanism. Second, Diana monkey alarm calls are based almost exclusively on this vocal production mechanism to an extent that has never been documented in mammalian vocal behavior. Finally, the Diana monkeys’ pulsed phonation strongly resembles the pulse register in human speech, where fundamental frequency is mainly controlled by subglottal pressure. Here, we report the results of a detailed acoustic analysis to investigate the production mechanism of Diana monkey alarm calls. Within calls, we found a positive correlation between the fundamental frequency and the pulse amplitude, suggesting that both humans and monkeys control fundamental frequency by subglottal pressure. While in humans pulsed phonation is usually considered pathological or artificial, male Diana monkeys rely exclusively on pulsed phonation, suggesting a functional adaptation. Moreover, we were unable to document any nonlinear phenomena, despite the fact that they occur frequently in the vocal repertoire of humans and nonhumans, further suggesting that the very robust Diana monkey pulse production mechanism has evolved for a particular functional purpose. We discuss the implications of these findings for the structural evolution of Diana monkey alarm calls and suggest that the restricted variability in fundamental frequency and robustness of the source signal gave rise to the formant patterns observed in Diana monkey alarm calls, used to convey predator information. I. INTRODUCTION mental frequency of the sound produced by the vocal folds is additionally directly related with the tension of the vocal fold The vocalizations of many mammals are the result of tissue ͑Titze, 1989, 1991͒. two distinct components: the oscillating vocal folds within Adult male Diana monkeys ͑Cercopithecus diana͒ pro- the larynx produce a primary acoustic signal, which then duce acoustically distinct alarm calls to two of their preda- undergoes a filtering process within the vocal tract where tors, the crowned eagle and the leopard ͑Zuberbu¨hler et al., various frequency bands are dampened to different degrees 1997; Zuberbu¨hler, 2000a͒. Playback experiments have ͑van den Berg, 1958; Fant, 1960; Titze, 1994; Owren and shown that nearby listeners respond to these alarm calls as if Linker, 1995͒. Basic vocal fold behavior can be described as the corresponding predator were present, suggesting that the following: Bernoulli forces cause the vocal folds ͑if close these calls inform nearby recipients about important ongoing to each other͒ to be sucked together, creating a closed air- events in the environment ͑Zuberbu¨hler et al., 1999; Zuber- space below the glottis. Continued subglottal air pressure bu¨hler, 2000b͒. Acoustically, the Diana monkeys’ alarm vo- from the lungs builds up underneath the closed folds. Once calizations consist of a bout of calls. Bouts vary in the num- this pressure becomes high enough, the folds are blown out- ber of calls from one to more than a dozen. Individual calls ward, thus opening the glottis and releasing a single ‘‘puff’’ are characterized by a highly stereotypic pulse pattern and ͑ ͒ of air ͑van den Berg, 1958͒. As the subglottal pressure in- calls are interspersed by short harmonic elements Fig. 1 . creases, two effects can be observed. First, the motion of the The single pulses within each call resemble a damped vocal folds becomes faster ͑demonstrated in computer mod- oscillation: a rapid, transient change in signal amplitude from els: Ishizaka and Flanagan, 1972; Steinecke and Herzel, a baseline value to a higher or lower value, followed by a 1995, and in vitro: Titze, 1989͒. Second, the sound pressure rapid return to the baseline value. Elsewhere, we showed that level increases ͑Gramming, 1988; Titze, 1994͒. The funda- the formant peak frequency and formant transition of the pulse elements is the single most important parameter to dif- ferentiate eagle versus leopard alarm calls ͑Riede and Zuber- a͒ Present address and address for correspondence: Tobias Riede, 315 Jordan bu¨hler, in press͒, suggesting that similar to human speech Hall, School of Medicine, Indiana University, Bloomington, IN 47405. Electronic mail: [email protected] sounds, some primate vocalizations convey important se- b͒Electronic mail: [email protected] mantic information by formant structures. Although research 2 completely adducted and a small vocal fold excursion ͑Hol- lien et al., 1977͒. The fundamental frequency is affected by different fac- tors in each of the three registers. In the modal register, the fundamental frequency is mainly determined by changes in vocal fold length and stiffness ͑Murry and Brown, 1971͒. Moreover, there is a positive correlation between vocal fold thickness ͑i.e., mass, length, and stiffness͒ and fundamental frequency ͓reviewed in Titze ͑1994͔͒. This relationship is absent in the pulse register ͑Hollien et al., 1969; Allen and Hollien, 1973͒. Instead, the fundamental frequency of the pulse register appears to be predominantly determined by changes in subglottal air pressure. To investigate the vocal production mechanism of the Diana monkey, we analyzed the relationship between call amplitude ͑a reliable estimator of subglottal pressure͒ and fundamental frequency. We predicted a positive relationship FIG. 1. Time domain and spectrogram of a leopard alarm bout, consisting of between these two parameters if Diana monkey alarm calls seven calls. Basic unit of the call is the pulse as shown in the ‘‘zoom in’’ picture of Fig. 2. are the product of the same source production mechanism that is responsible for the human pulse register. on the structural evolution of animal vocalizations is not new A second aim of this study was to investigate the role of ͑Morton, 1977͒, comparatively little is still known about how nonlinear phenomena in the vocalizations of Diana monkey natural and sexual selection affected the acoustic structure of alarm calls. Nonlinear phenomena are relevant in this context primate alarm calls ͑Zuberbu¨hler, 2003͒. Here, we provide a because they can be directly related to events at the laryngeal detailed acoustic analysis of the source characteristics of Di- source. Several lines of research suggest that nonlinear phe- ana monkey alarm calls to elucidate the adaptive significance nomena are common and ubiquitous in mammalian vocaliza- tion behavior ͑Wilden et al., 1998; Mergell et al., 1999; and physiological constraints of this remarkable vocalization. ͒ Human speech sounds can be produced using three dif- Riede et al., 1997, 2000; Fischer et al., 2000 . Phenomena ferent registers. A register can be described by the frequency such as frequency jumps, subharmonics, biphonation, and range covered and by the specific mode of vocal fold behav- deterministic chaos are commonly observed, usually the re- ior by which it is produced ͑e.g., Hollien, 1974; Titze, 1994; sult of deviations from the regular harmonic vibration pattern Svec et al., 1999͒. Although each register covers a certain of the vocal folds, such as nonsynchronously oscillating left and right vocal folds or simultaneously oscillating horizontal frequency range, neighboring registers overlap significantly. ͑ Normal speech is delivered in the so-called modal ͑or chest͒ and vertical components of the vocal folds e.g., Herzel ͑ ͒ et al., 1994; Berry, 2001; Berry et al., 1994; Steinecke and register fundamental frequency range 100–300 Hz . Hu- ͒ mans are also capable to produce speech using either the Herzel, 1995; Tigges et al., 1997; Neubauer et al., 2001 . falsetto ͑or flagolet͒ register ͑fundamental frequency Ͼ300 The two combined approaches are likely to yield important Hz͒ or the pulse ͑or vocal fry͒ register ͓fundamental fre- insights into the sound production mechanism underlying quency Ͻ100 Hz ͑Blomgren et al., 1998͔͒. Recent studies male Diana monkey alarm calls. suggest the existence of a separate fourth register, i.e., the vocal-ventricular phonation mode, like pulse register cover- II. MATERIAL AND METHODS ing the frequency range below 100 Hz but unlike pulse reg- A. Study site and subjects ister involving the ventricular folds ͑‘‘false folds’’͒ into the mode of production ͑Fuks et al., 1998; Lindestad et al., Data were collected in an approximately 40-km2 study- 2001͒. According to this terminology we used the term area of primary rain forest surrounding the Centre en ‘‘pulse register’’ to describe the Diana monkey calls, because Recherche d’Ecologie ͑University of Cocody, Abidjan͒ re- these vocalizations strongly resemble the pulse register of search station ͑5°50ЈN, 7°21ЈW͒ in the Taı¨ National Park, humans ͓see
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